BOTANY LETTERS https://doi.org/10.1080/23818107.2020.1864470

Monographs on invasive plants in Europe N° 4: Arundo donax L. Jesús Jiménez-Ruiz a,b, Laurent Hardion c, Juan Pablo Del Monte a, Bruno Vila d and M. Inés Santín- Montanyá b

aEscuela Técnica Superior de Ingeniería Agronómica, Alimentaria y de Biosistemas, Universidad Politécnica de Madrid (UPM), Madrid, Spain; bSubdirección General de Investigación y Tecnología, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), Ministerio de Ciencia E Innovación, Madrid, Spain; cLaboratoire Image Ville Environnement, Université de Strasbourg, CNRS, Strasbourg, France; dLaboratoire Population Environnement Développement, Aix-Marseille Université, IRD, Marseille, France

ABSTRACT ARTICLE HISTORY Arundo donax L. (Poaceae) is considered to be one of the worst invasive plants in the world, and Received 14 January 2020 here, we present a synthesis of all aspects of its biology, ecology and management that are Accepted 23 November 2020 relevant to understanding its invasive behaviour. This report presents information on the KEYWORDS taxonomy, morphology, distribution, history of introduction and spread, ecology, responses Biology; ecophysiology; to abiotic and biotic factors, biology, negative impacts, management and uses within the ecological interactions; giant framework of a series of Botany Letters on Monographs on invasive plants in Europe. Arundo reed; genetic diversity; donax (giant reed) originated in subtropical Asia and is invasive in other warm regions world­ invasive species; invasion wide, especially in degraded riparian areas. Introduced for use in agriculture, erosion control history; management; and construction in the Mediterranean European region since ancient times, it has become negative impacts; Poaceae; naturalized in several freshwater habitats and in disturbed areas. In its introduced range, reproductive biology; uses A. donax shows strong genetic uniformity and no seed production. This situation is reversed in Asia, where this taxon is fertile and morphologically and genetically polymorphic. This perennial grass combines rhizomatous clonal growth with a tolerance to a wide variety of ecological conditions, such as high salinity levels and long droughts. This tall reed can increase the risk of fire, alter the natural drainage of channels and invade very sensitive habitats, posing a serious threat to riparian habitats and freshwater ecosystems. Effective methods to control A. donax are tarps on a cleared giant reed field to completely cover the affected zone, rhizome removal using a modified backhoe bucket adapted to separate soil from the rhizomes, and herbicide application on leaves. The combined technique of herbicide treatment plus stem- cutting can be included in management programmes, and this technique needs to be mon­ itored over the long term to assess its success and to ensure native species colonization and ecosystem recovery. Regarding biological control, A. donax is host to different insect species that have been released to control it in parts of its non-native range (North America) with some success. However, these differentmethods of control should continue to be studied, evaluating the risks posed to the environment and the control level achieved. In this context, scientific, political and administrative efforts as well as environmental education are effective assets to address the management of this invasive species.

1. Taxonomy terms signifying “reed”, the genus name Arundo that seems to be of Latin origin (used by Virgil) and the 1.1. Names and classification epithet donax from the Greek δόναξ (used by Scientific name: Arundo donax L., 1753 Theophrastus). This species is the type of the genus Taxonomic position: Monocotyledons; Order: Arundo L., which is the type of the Arundinoideae Poales; Family: Poaceae; Subfamily: Arundinoideae Kunth ex Beilschm. subfamily. The species is placed Kunth ex Beilschm.; Tribe: Arundineae Dumort. in the Arundineae Dumort. tribe, despite the highly Common names: Spanisches Rohr, Pfahlrohr [DE], heterogeneous composition of this tribe according to giant reed, Spanish cane, bamboo reed [EN], Spaanse- molecular phylogenies (Hardion et al. 2017a, 2017b). riet [NL], caña de techar, caña de la reina, caña de Linnaeus described this species from Spain and France Castilla, carrizo grande, caña común, caña india [ES], (“Habitat in Hispania, Galloprovincia”). The lectotype Canne de Provence [FR], canna commune, canna designated (Jarvis et al. 1993) is conserved in domestica, canna gentile [IT], cana-do-brejo, canno- L Herbarium, Leiden, Nederland (Herb. A. van do-reino, capim-plumoso, cana-do-reino [PT] Royen No. 912.356–93). Among the numerous syno­ EPPO code: ABKDO nyms of Arundo donax, several are due to the descrip­ Arundo donax L. (Poaceae) was described by Carl tion of improperly named genera such as Amphidonax Linnaeus in Species Plantarum (1753), based on two Nees, Donax P. Beauv., and Scolochloa Mert. & W.D.J.

CONTACT Jesús Jiménez-Ruiz [email protected] Escuela Técnica Superior de Ingeniería Agronómica, Alimentaria y de Biosistemas, Universidad Politécnica de Madrid (UPM), Campus, Av. Puerta de Hierro, n° 2, 4, 28040, Madrid, Spain © 2020 Société botanique de France

Published online 03 Jan 2021 2 J. JIMÉNEZ-RUIZ ET AL.

Koch. Arundo sativa, one of the synonyms of Arundo donax described by Lamarck, exemplifies its human use (cf. 6. Uses). Several other taxa described in Asia, where populations are characterized by larger mor­ phological and genetic variation (Hardion et al. 2014), are now considered synonyms of A. donax: A. bifaria Retz., A. bengalensis Retz. and A. coleotricha (Hack.) Honda (= A. donax var. coleo­ tricha Hack.). An extensive taxonomic revision of Asian populations would be necessary to resolve the systematic ambiguity. The most cited varieties of this species are A. donax var. versicolor (Mill.) Stokes (= A. donax var. variegate Vilm.), describing a phenotype with variegated leaves often used as an ornamental plant. The mention A. donax var. macrophylla in recent literature should correspond to the cultivar A. donax “Macrophylla” with broad leaves. Among the genus Arundo, four other species are currently accepted (Hardion et al. 2012): the circum- Mediterranean A. micrantha Lam., the Italo-Balkan A. plinii Turra, the Ligurian A. donaciformis (Loisel.) and the Taiwanese A. formosana Hack.

1.2. Morphological description Figure 1. The giant reed, Arundo donax L. (Poaceae), with ~5 m high flowering culms. The present description only considers the clonal lineage of A. donax that occurs in the Mediterranean Basin and is invasive in other first year) to yellowish (when branching), with warm regions worldwide, widely described in a mean internode length of approximately 10 cen­ European floras (e.g. Bolòs and Vigo 2001), without timetres and glabrous nodes supporting one leaf consideration of native populations occurring in and one bud. These nodes can also easily produce Asia. The invasive A. donax is a rhizomatous geo­ adventive roots and new culms with tillering or phyte, producing robust culms measuring up to culm fragmentation. Leaves possess glabrous 6 m high (Table 1). Culms could be pluriannual, sheaths split to the base and a large glabrous limb with a main axis flowering the first year and pro­ (up to 6 centimetres) with hairy yellowish auricles. ducing ramifications the following years. This spe­ The ligule is very short (1 mm), membranous and cies forms dense clumps due to the reduced length briefly ciliate. The inflorescence is a large panicule of its rhizome internodes (Figure 1). The rhizome consisting of approximately one thousand spikelets. is solid and thick. Culms are sea green (the This panicle opens at the end of the summer and then compresses after pollination. The spikelet con­ Table 1. Morphological parameters for Arundo donax esti­ tains two glabrous glumes of equal lengths and mated on 165 culms from 11 Mediterranean localities (Data three to five florets. Each floret possesses one aris­ from Hardion et al. 2012). tate lemma (c. 11 mm long) with long hairs (c. st th 1 – 4 5 mm) inserted on the first quarter and a smaller Variables mean ± SD quartiles min – max Culm heighta 4.8 ± 6.7 4.4–5.2 3.1–6.2 palea (c. 7 mm) with a truncated apex. The lemma Panicule lenghtb 53.4 ± 11.9 44.5–61.5 23.5–79.2 also possesses two short teeth at the base of the c Culm diameter 24.2 ± 4.5 21.0–27.3 13.0–35.7 terminal awn, which often look like tears between Number of nodes per culm 41.7 ± 4.7 39.0–45.0 26.0–52.0 Leaf lengthb 57.0 ± 12.4 48.0–64.5 22.2–93.0 the three lemma ribs. Maximal leaf widthb 5.8 ± 1.5 4.7–6.8 1.5–10.1 Culm internode lengthb 10.1 ± 1.8 8.7–11.3 5.8–14.6 c Rhizome diameter 32.1 ± 8.5 26.8–38.1 11.7–52.0 1.3. Distinguishing features Rhizome internode 7.7 ± 0.3 5.0–1.0 2.0–19.0 lengthc Lower glume lengthc 11.2 ± 1.1 10.4–12.1 9.5–13.5 In Europe, A. donax is often confused with other Upper glume lengthc 11.1 ± 0.7 10.5–11.5 9.9–12.5 Mediterranean Arundo spp. or even with Phragmites Lemma lengthc 11.2 ± 0.9 10.5–11.6 9.0–13.3 Palea lengthc 6.7 ± 0.5 6.4–7.1 5.0–7.4 species. Therefore, Table 2, Figures 2 and Figures 3 Lemma hairs lengthc 5.6 ± 0.3 5.4–5.8 5.0–6.1 summarize several distinguishing features that can be ain m; bin cm; cin mm used to differentiate them. BOTANY LETTERS 3

Table 2. Comparative characters to distinguish Arundo donax from other Mediterranean Arundo and Phragmites. Arundo donaxa Arundo micrantha Arundo pliniib Phragmites spp. Glumes equal equal equal unequal Lemma hairsc on its 1st quarter at its 1st quater at its 1st quater on the pedicel Florets per spikelet 3–5 1–2(3) 1–2(3) 3–10 Panicle shaped erect erect erect drooping Stem nodes glabrous glabrous hairy hairy Leaf ligule short membranous short membranous short membranous ciliate Leaf auricule large medium medium short to absent Leaf sheath glabrous poorly hairy hairy hairy Leaf directiond bilateral bilateral bilateral often unilateral Rhizome thicknesse thick thin thin thin Rhizome internodee < 1 cm > 1 cm 1 cm 1 cm Rhizome sectione solid hollow hollow hollow with aerenchyma aonly considering the Mediterranean morphotypes; bincluding A. donaciformis for these characters; csee Figure 3; da character to observe well after anthesis; esee Figure 2.

2. Distribution and status varieties currently hidden under the name A. donax. In fact, Hardion et al. (2014) described the phyloge­ Arundo donax is widespread in tropical and subtropi­ netic origin of the invasive clonal lineage in the Middle cal regions worldwide (Figure 4) and even in tempe­ East (Pakistan and Afghanistan). However, three other rate regions but rather under cultivated conditions. It lineages were also detected along Himalayan slopes is widely dispersed and naturalized in all similar cli­ (India and Nepal) and in China (based on plastid mates in many regions of the world, including south­ DNA markers). Very few publications from Asian ern Africa, the USA, Mexico, the Caribbean, South authors focus on the species, and it appears not threa­ America and the Pacific Islands (Häfliger and Scholz tened and not in decline in its native range. Based on 1981). the literature, A. donax is probably native to the fol­ lowing countries: 2.1. Native range Asia: Bangladesh, Bhutan, Japan, Pakistan, Thailand, Afghanistan, Cambodia, China, India, Iran, The exact native range of Arundo donax is still Laos, Malaysia, Myanmar, Nepal, Turkmenistan, a controversial issue since different authors suggest Uzbekistan, and Vietnam. that its origin is the Middle East or Eastern Asia (Polunin and Huxley 1987) and other scientists sug­ gest a Mediterranean origin (Zeven and Wet 1982). 2.2. Introduced range This second hypothesis was discredited given the extensive clonality and sterility of A. donax in the Currently, A. donax has been introduced in several warm Mediterranean (Hardion et al. 2012). In the Old countries worldwide (Figure 4), but it is considered an World, A. donax is considered native from Asia invasive species mainly in countries with a subtropical or (Middle East and East Asia), where this species pre­ Mediterranean climate. As a result, among the dozens of sents a larger morphological variation than that in publications addressing the invasiveness of A. donax, other areas. In this area, species taxonomy should be a large majority of them were published by US institu­ revised to test the occurrence of other species or tions, and the others were mainly published by

Figure 2. Rhizome features distinguishing (a) Phragmites australis with cortical aerenchyma, (b) Arundo donax with solid rhizome, and (c) Arundo plinii with a reduced lumen within a thick parenchyma. 4 J. JIMÉNEZ-RUIZ ET AL.

Figure 3. Floret features distinguishing (a) Phragmites australis with lemma hairs inserted on the rachilla, (b) Arundo donax with long hairs inserted all along the basal quarter of the lemma, and (c) Arundo plinii with long hairs inserted in a ring at the first quarter of the lemma.

Figure 4. Distribution of Arundo donax among native (green) and introduced (red) range. Hatched areas correspond to countries for which this status is questioned or debated in the literature.

Mediterranean, South African and Australian institu­ distribution demonstrates its substantial human tions. According to the Global Invasive Species use. Arundo donax has always been considered an Database and other literature, A. donax could be consid­ alien species in the New World. It was initially ered an invasive species in the following countries – the introduced into southern California from the list also includes Mediterranean countries where Mediterranean in the 1820s for numerous uses (e.g. A. donax has been invasive for a very long time: erosion control, musical instruments, and farming) Africa: Algeria, Morocco, South Africa, Swaziland, before its rapid spread in riparian habitats (Bell and Tunisia. 1997). It is also considered an invasive species in America: Brazil, Dominican Republic, Haiti, South Africa, where it was introduced in the late Mexico, and the USA. 1700s for erosion control (Canavan et al. 2017). In Europe: France, Portugal, Spain, Italy, Greece, and Australia, it was introduced during the 19th century Romania. (Haddadchi et al. 2013). Oceania: Australia, Fiji, French Polynesia, Micronesia, New Caledonia, and New Zealand. 3. Ecology 2.3. History of introduction and spread 3.1. Response to abiotic factors In the Mediterranean Basin, this species was 3.1.1. Climate recently described as an invasive archaeophyte (i.e. Giant reed is extremely tolerant to different climates species introduced before 1500 AD; Hardion et al. (Perdue 1958), surviving and growing under a wide 2014), which invaded riparian ecosystems and variety of temperature and rainfall conditions human disturbed lands several hundred years ago. (Mariani et al. 2010) with however a preference for Currently, it has become a structuring species of warm and subtropical climates (2019). Its regeneration Mediterranean lowland landscapes, and its large is very sensitive to temperature, implying that BOTANY LETTERS 5

A. donax development is limited in areas with very Santa Clara River in southern California, found that cold winters. Although this species can tolerate low the growth of A. donax was greater than that of native temperatures during the dormancy phase, if frost plants. On average, giant reeds grew 3 to 4 times faster occurs once growth has begun during the spring, in height than native riparian plants, up to 2.62 cm/ then the frost severely damages the plant (Perdue day (average 0.72 cm/day), and reached up to 2.3 m in 1958; Dudley 2000; Decruyenaere and Holt 2001). height in less than 3 months after a fire.Arundo donax According to Spencer and Ksander (2006), below 7° density was approximately 20 times higher and pro­ C, the rhizome stops producing new shoots (ramets), ductivity was 14–24 times greater than those of native while above 30°C, shoot inhibition occurs. Regarding plants one year post-fire. This fast growth after fire precipitation, A. donax tolerates values between 300 events is one way how A. donax can change ecological and 4000 mm (Duke 1975). In addition, this invasive interactions in riparian ecosystems, which change plant has been found to colonize high altitudes, up to from being habitats regulated by floods to habitats 4000 m in Central America (Tropicos database 2007). regulated by fire that are structurally simpler and more homogeneous (Deltoro Torró et al. 2012). 3.1.2. Soil moisture, soil pH, salinity and nutrients Arundo donax is considered an emergent aquatic plant 3.2. Response to biotic factors (Cook 1990) or a hydrophyte that needs a certain degree of soil moisture for its initial establishment Arundo donax is capable of invading differenthabitats; (Bell 1997). However, the plant is capable of coloniz­ however, it most often invades riparian habitats ing an entire riparian area, from the riverbank to because these habitats have high levels of nutrients higher elevation areas with low soil moisture values and disturbances, providing the best conditions for where the riparian forest changes completely the establishment of this species. Disturbances com­ (DiTomaso and Healy 2003). The ability of A. donax monly occur in riparian zones and generate areas to grow under water-deficient conditions is due to the without competition that are particularly vulnerable rhizomes penetrating deep soil layers to obtain the to being colonized by A. donax (Planty-Tabacchi et al. existing moisture. This trait allows giant reed to be 1996; Boland 2006). In the more vegetated parts of resistant to drought conditions (Sher et al. 2003). After riparian habitats, the erect and branched shape of the first year of growth, A. donax becomes relatively woody native plants may restrict the expansion of tolerant to drought but also survives in very wet and A. donax. However, the higher productivity of saline soils (Pilu et al. 2012). Arundo donax is capable A. donax even in situations in which it is diminished to tolerate high electrical conductivities in the soil by competition with native species suggests eventual water of 35–45 dS m−1 (i.e. extremely saline condi­ competitive exclusion of native species, as confirmed tions) and to produce a high yield under these condi­ by Quinn and Holt (2009). In summary, woody spe­ tions when used as a bioenergy crop, leading some cies can to some extent limit the extension of A. donax authors to consider it a halophyte plant (Williams (see also section 6.7 Ecological control and restoration) et al. 2008; Williams and Biswas 2009). but there is overall little biotic resistance to its estab­ Arundo donax is indifferent to the mineralogical nat­ lishment. Conversely, A. donax can exclude native ure of a substrate (Perdue 1958), being able to grow in species due to its high productivity levels based on its clay, sandy or stony soils, even semi-saline estuaries physiology and its clonal growth, which allows it to (Grossinger et al. 1998; Quinn and Holt 2008), and occupy the substrate vertically (stems) and horizon­ tolerates a soil pH ranging from 5.0 to 8.7 (Duke tally (rhizomes). 1975). According to Rieger and Kreager (1989), A. donax is always observed occupying riverbanks 3.3. Habitats and syntaxonomy with high nutrient contents. In its native area, A. donax grows along lakes, streams, 3.1.3. Fire drains and other wetlands near water because it needs Arundo donax presents high productivity (high a high supply of water in its first growth stages (Bell growth rate), consolidating its dominance in riparian 1997). In general, its preferred habitats range from ecosystems since it is able to regrow immediately after moist well-drained soils to those with a water table at fire and faster than native vegetation (Bell 1993). One or near the surface and disturbed areas such as river­ possible explanation of its dominance is the accumu­ banks (Ewel et al. 2001). lation of reserves in the rhizomes, which are not In Europe, the most common habitats of giant affected by fire (Coffman 2007). In addition, this spe­ reeds are riparian zones of river basins and include: cies can use very effectively the elevated nutrient soil i) riparian environments and wetlands along tempor­ levels post-fire released by mineralization during the ary (EUNIS habitat code C2.5) or permanent water fire (Zedler et al. 1983). Coffman et al. (2010), in courses (EUNIS habitat codes C2.2 and C2.3), ii) sea­ a study carried out in riparian woodlands along the sonally flooded grasslands on sub-saline soils (EUNIS 6 J. JIMÉNEZ-RUIZ ET AL. habitat code E.3), and iii) retrodunal depressions biological control agent producing galls in the stems (EUNIS habitat code B1.4). In the Mediterranean and lateral shoots (Claridge 1961; Goolsby and Moran area, the largest A. donax populations occur in ripar­ 2009; Moran and Goolsby 2009). Rhizaspidiotus dona­ ian areas and floodplains, from wet sites to dry river­ cis Leonardi (Hemiptera: Diaspididae) is another insect banks far from permanent water in terrestrial identified with a high potential impact on the growth of ecosystems (Deltoro Torró et al. 2012). In addition, the giant reed (Moore et al. 2010; Cortés et al. 2011a, this species is common in agricultural habitats along 2011b). In southern California and northern Mexico, field borders (EUNIS habitat code I), especially in the shoot fly Cryptonevra sp. (Diptera: Chloropidae) ditches, grasslands (EUNIS habitat code E5.44), rud­ and the aphid Melanaphis donacis Passerini eral areas, disturbed areas, roadsides and urban zones (Hemiptera: Aphididae) (Dudley and Lambert 2007) (EUNIS habitat code J) (Sanz Elorza et al. 2004). are particularly common on Arundo-infested sites. In According to the database of the European Nature France, Phothedes dulcis Oberthür (Lepidoptera: Information System (EUNIS 2020), the habitat classi­ Noctuidae) has been recorded feeding on giant reeds fication for A. donax is described as “Arundo donax (Dufay 1979). A moth borer Diatraea saccharalis beds” with the EUNIS habitat code C.3.32. and Fabricius (Lepidoptera: Crambidae) has been reported described as “very tall thickets of Arundo donax lining attacking the lateral shoots and stems of giant reeds in water courses of the Middle East and Central Asia; Barbados (Tucker 1940), and A. donax is an important similar formations of the Mediterranean basin, where food source for Zyginidia guyumi Sohi and Mann the species is an old introduction, are included”. (Typholocyloinae: Cicadellidae) in Pakistan (Ahmed In the USA, A. donax can be found in several places et al. 1977). In South Africa, through field surveys where it was planted for erosion control in the early and a literature review, Canavan et al. (2017) observed 1800s (Mariani et al. 2010), such as in California and 13 herbivores feeding on A. donax populations, with in Texas, along the Rio Grande River with an abun­ two specialist herbivores from its native range, and dant naturalized population, where it invaded riparian shared native herbivores with Phragmites spp. The ecosystems (Häfliger and Scholz 1981). In California, most widespread insect found in South Africa was the establishment of A. donax after flood events was Tetramesa romana. Other invertebrates that have studied by Else (1996), who showed the highest been recorded feeding on stems, shoots and leaves deposition and establishment frequency occurring on were Dimorphopterus zuluensis Slater (Hemiptera: depositional bars and not in the permanent water Lygaeidae), Melanaphis donacis, Hyalopterus pruni channel. In Central and South America, it is also Geoffroy (Hemiptera: Aphididae), Haplothrips gowdeyi very common to find giant reeds invading riparian Franklin (Thysanoptera: Phlaeothripidae), Chilo partel­ systems and wetlands (Flores Maldonado et al. 2008). lus Swinhoe (Lepidoptera: Crambidae), Sesamia capen­ In Oceania, particularly in Australia, and in South sis Le Ru and Sesamia calamistis Hampson Africa, A. donax occurs as a weed in waterways, drai­ (Lepidoptera: Noctuidae), Busseola fusca Fuller nage lines, swampy areas, roadsides, wet disturbed (Lepidoptera: Noctuidae), one species of the order sites, waste areas, old gardens and urban bushlands Diptera (Chloropidae) and one species of the order in temperate, subtropical and tropical environments Coleoptera (Curculionidae) (Canavan et al. 2017). (Canavan et al. 2017). The insect species T. romana (Arundo wasp) and R. donacis (Arundo armoured scale) have shown the most promising features as biological control agents 3.4. Ecological interactions (see 6.6. Biological control) and host specificity for Arundo donax leaves contain a number of toxic and giant reeds (Goolsby and Moran 2009). unpalatable natural minerals and chemicals, such as silica, cardiac glycosides, and alkaloids, that protect the plant from native insects (Bell 1993). In general, 4. Biology the presence of these toxic chemicals and minerals 4.1. Phenology protects the plant from predators that might attempt to feed or reproduce on it. Despite this, a variety of The phenological cycle starts with new shoots emer­ insect herbivores have been found to be associated with ging from rhizomes in spring. Towards the end of A. donax plants in North America, in the August, the lower leaves of the giant reed in their Mediterranean area of Europe, South Africa and across first year of life begin to dry (Saltonstall et al. 2010). southern Asia (Kirk et al. 2003; Goolsby and Moran This process continues during autumn, when the 2009; Cortés et al. 2011a; Canavan et al. 2017). One of water content of the aerial part decreases, in parallel the most commonly associated species is Tetramesa to a gradual lignification, with a loss in green colour romana Walker (Hymenoptera: Eurytomidae), the and a reduction in its physiological activity (Zembal Arundo wasp, which is an insect monophagous to the and Hoffman 2000). This process is due to progres­ Arundo genus (A. donax and A. plinii) and a potential sively lower temperatures, among other factors (Wijte BOTANY LETTERS 7 et al. 2005; Pompeiano et al. 2019). In addition, in this withstanding long periods of drought accompanied by season, flowering takes place, and the stems appear alternating periods of low and excessive humidity crowned by feathery inflorescences. These processes (Perdue 1958), as well as being able to grow in semi- are accompanied by a transport of soluble carbohy­ arid habitats (Hoshovsky 1987). This drought- drates through the phloem, from the aerial part to the resistance ability of A. donax is due to the thickness subterranean storage organs, which translates into of its stems and to its rhizomes since its roots can a lower content of these compounds in the leaves in penetrate to deep depths and can reach the existing autumn than in spring and summer (Decruyenaere moisture in those layers (Else and Zedler 1996). and Holt 2001). In fact, there is an alternation in Another trait that plays an important role in its A. donax between the allocation of nutrients to the drought response is the capacity of the giant reed to aerial part in spring and summer and to the under­ retain a high degree of leaf-level net photosynthesis ground part in autumn and winter (Dudley 2000). rate (Pn), producing new shoots that quickly become A. donax blooms at the end of summer, between independent of rhizome reserves once they emerge August and October, although the seeds it produces and gain biomass under water-deficitstress conditions are not fertile in its introduced range (Lewandowski (Haworth et al. 2016). These plant characteristics et al. 2003). After winter, with the start of the second make it capable of growing in drylands (Perdue growing season, the lateral branches are emitted from 1958). However, Mann et al. (2013) suggested that the axillary buds present in the nodes (Decruyenaere giant reeds are affected by drought conditions (mild and Holt 2001). These branches constitute 75% of the and severe droughts) during the first year of growth. leaf area of a mature A. donax plant. In another study carried out in the Mediterranean area to evaluate the effect of drought tolerance at early stages, the plant growth and leaf gas exchange para­ 4.2. Physiological data meters of A. donax were significantly affected as soil 4.2.1. Response to nutrient availability water availability decreased to less than 40% (Romero- Nutrient enrichment in riparian areas has led to Munar et al. 2014). These results suggest that although numerous invasive species invading these ecosys­ giant reeds are able to grow under water-stress condi­ tems (Hood and Naiman 2000; Richardson et al. tions, drought can affect them significantly in the ear­ 2007). In addition to nutrient-rich alluvial deposits, liest growth stages, when the plants need a certain the generalized use of fertilizers and the abundant degree of soil moisture for establishment (Pilu et al. deposition of organic matter originating from 2012; Webster et al. 2016). anthropic activities (agriculture, livestock, waste­ Mann et al. (2013) studied the effect of flooded water, etc.) cause these environments to become conditions on newly planted rhizome fragments to ideal areas for the establishment and growth of characterize the environmental tolerance of giant A. donax (Jiménez-Ruiz et al. 2011). According to reed under greenhouse conditions. These results sup­ Quinn et al. (2007) and Jiménez-Ruiz et al. (2011), port the hypothesis that A. donax needs adequate soil the growth of A. donax is modulated by nutrient moisture to become established (early stages), but availability. In sites with high nitrogen concentra­ prolonged and heavy flooding is also harmful to the tions, A. donax does not exhibit dormancy and the survival of young plants throughout their first year mass of rhizomes expands actively laterally, which (Bell 1993). constitutes a competitive behaviour (Coffman 2007). In contrast, in nutrient-poor environments, 4.2.3. Response to light availability A. donax growth is more conservative, limited to According to Spencer et al. (2005), Arundo donax replacing old stems and exhibiting a period of tolerates low levels of radiation and it is able to persist dormancy during the winter (Decruyenaere and and grow under intermittent and low-light conditions, Holt 2005). which implies that the plant could take advantage of In addition, giant reeds have been shown to experi­ sun flecks within the resident plant community ence a positive effect from nitrogen addition, as it (Spencer 2012). Other results have suggested that increases their height and results in more rapid root shade may hinder its establishment on riverbanks growth (Sher et al. 2003; Coffman2007 ). In the natural (Coffman 2007). Its ecological optimum seems in any environment, Boland (2006) observed similar results case to be in full light conditions: in environments in that rhizomes in flooded areas that were rich in with high light intensity, nutrients and water water and nutrients grew faster than those in environ­ resources, the highest growth rates of A. donax were ments with less water and nutrients. as high as 20 tons of dry weight per ha (Perdue 1958). Under these conditions, giant reed sprouts exhibited 4.2.2. Response to drought and flooding increases in length of up to 10.2 centimetres per day Arundo donax does not need a constant supply of (Dudley 2000). This rapid development is because all water (Gasith and Resh 1999) since it is capable of the growth of the giant reed is invested in 8 J. JIMÉNEZ-RUIZ ET AL. photosynthetic tissues with high photosynthetic capa­ as by asexual reproduction (Johnson et al. 2006). city (Rossa et al. 1998) and is supported by high water According to Boland (2006), the expansion by vegeta­ consumption. tive growth is the result of two processes: (a) The growth of the rhizomes, which is consid­ ered the main trait responsible for the local expansion 4.3. Reproductive biology of A. donax (Else and Zedler 1996; DiTomaso 1998). Arundo donax is considered sterile (i.e. non- The expansion of the plant in this way is a slow process fructiferous) throughout its whole introduced range. with a mean expansion of the basal edge of only Hundreds of spikelets were examined for seed produc­ 0.29 ± 0.04 m2 per year (Boland 2006). tion in the USA and in the Mediterranean without (b) The rooting of lignified stems. Boland (2006) success (Johnson et al. 2006; Hardion et al. 2015). demonstrated in a fieldstudy that stems on the ground Almost every node that is free of apical dominance is and rooted stems are capable of growing up to 7.4 able to produce a new stem. Its sterility is due to the times faster than rhizomes in areas subject to distur­ defective development of the male and female game­ bances due to floodsthat occur in riparian ecosystems. tophytes. In anthers, Balogh et al. (2012) observed that Although stem fragments may play a role in the fewer than 10% of microsporocytes go through meio­ dispersal of A. donax, rhizome fragments are mainly sis, and only some microspores (early stage pollen responsible for this process (Decruyenaere and Holt grains) were observed in older anthers. Hardion et al. 2001; Quinn 2006). The dispersal of A. donax is helped (2015) observed numerous sclerified and empty by fragments of rhizomes that can produce new shoots anthers, and some anthers contained few collapsed under a wide range of rhizome sizes and the vast pollen grains without cytoplasm. Among the multi­ majority of environmental conditions, and in compar­ tude of abortive pollen grains, Mariani et al. (2010) ison to stem fragments, rhizomes retain the ability to observed some normal forms, but none of these three regrow for a much longer period (Decruyenaere and studies observed germination of a pollen tube for the Holt 2001; Quinn 2006). In relation to the rhizome invasive A. donax. Balogh et al. (2012) observed fewer fragments and their size, Santín-Montanyá et al. than 10% of the ovaries enlarging as mature caryopses. (2014) carried out a study in greenhouse conditions However, none of these pseudo-caryopses produce to determine the production of new shoots by different seedlings under various growth conditions. In effect, rhizome sizes (<1 cm, 1 cm, 3 cm, and 5 cm) of giant microscopic examinations of ovule development reed in Spain. Only, shredded rhizomes of fragments stages revealed early failure of megasporocyte devel­ size ≤1 cm were not able to regrow (Santín-Montanyá opment. Mariani et al. (2010) also observed failure of et al. 2014). The production of fragments (rhizomes or megasporogenesis but at the next stage. In its native stems) that allow dispersion and colonization over range, Arundo donax produces seeds in Iran, long distances is a rare phenomenon under natural Afghanistan, Pakistan, India, Nepal and Bhutan conditions, even under favourable conditions for its (observations of herbarium samples; Hardion et al. generation, such as intense rainfall and the resulting 2014). floods(Boland 2006, 2008). The high rates of fragment The invasive clonal lineage of A. donax possesses production described in the literature (Else and Zedler 2n = c.108–110 (http://ccdb.tau.ac.il). Even if this num­ 1996) are due to mechanical removal of the species, ber indicates a high ploidy level, the smaller chromosome such as the extraction of rhizomes and their subse­ number described in Arundo is 2n = c.72, e.g. for Asian quent crushing together with the aerial part. populations of A. donax (Larsen 1963; Christopher and Abraham 1971; Mehra and Kalia 1975; Kalia 1978). The 4.5. Genetic diversity invasive A. donax is most likely a pseudo-triploid form generated from native populations with 2n = 72. Such Most of the 12 phylogenetic studies focusing on triploid formation should be recurrent, as observed in Arundo donax show low or no genetic diversity in A. plinii (Hardion et al. 2015). The whole genus Arundo the invaded range (including the Mediterranean) and probably diversified after such events of demi- genetically variable individuals in Asia (Table 3). duplication from 2n = 48 to 2n = 72 (Jike et al. 2020). Based on plastid mini- and microsatellites, Hardion et al. (2014) found the nearest relative of the invasive clone of A. donax in a Middle East lineage distributed 4.4. Local expansion and long-distance dispersal along the Indus Valley. They also found three other The main extension strategy of the invasive clonal lineages along the Himalayan slopes and in China. lineage is vegetative multiplication by rhizome growth Ahmad et al. (2008) documented the occurrence of or stem fragmentation. In the absence of fertile seeds only one genotype across the southern USA using in the non-native area, the local expansion of giant SRAP markers, Hardion et al. (2012) documents reeds is supported mainly by vegetative growth (new a genotype in the Mediterranean with AFLPs, and stems generated remain connected at all levels) as well Canavan et al. (2017) documented a genotype in BOTANY LETTERS 9

Table 3. Review of 12 molecular studies estimating the genetic diversity of Arundo donax. Authors Date Markers Sampling Genetic diversity Number of geno-types or lineages Khudamrongsawat et al. 2004 Isozymes, RAPD California (USA) Moderate - Ahmad et al. 2008 SRAP, TE USA Null 1 Mariani et al. 2010 AFLP Mediterranean; Asia Low; moderate 1; ≥ 1 Hardion et al. 2012 AFLP Mediterranean Null 1 Haddadchi et al. 2013 ISSR SE Australia Moderate 1 Tarin et al. 2013 nSSR N America; Mediterranean Low; high 6; 129 Zeng et al. 2013 ISSR China High 3 Hardion et al. 2014 cpDNA Mediterranean; Asia Null; high 1; 3 Pilu et al. 2014 SSR, maize genes Italy Low 3 Touchell et al. 2016 ISSR USA; Nepal Low; moderate 1; 2 Canavan et al. 2017 nSSR, cpDNA South Africa Null 1 Malone et al. 2017 AFLP SE Australia Low 2 SRAP, sequence-related amplification polymorphism; TE, transposable elements-based markers

South Africa with SSRs. Using AFLP, Malone et al. made of A. donax stems (Fernandes and Mendoça de (2017) showed the occurrence of two lineages in Carvalho 2004). In agriculture, these stems have been Australia, which may have been the gathering of an used to support orchard crops that are climbers, to invasive clone, and another Asian lineage expanded prop up branches, and to stake tomato plants. through Indonesia. Based on the SSRs in the maize Additionally, the stems can be used to hit trees genome, Pilu et al. (2014) found some genotypic dif­ (olive, almond, etc.) to harvest and to collect fruits ferences in Italy, without geographical structuring. In (Martínez et al. 2014). As a construction material, contrast, Tarin et al. (2013) found a very high genetic the stems are used to build structural elements or diversity in the Mediterranean (129 genotypes from agglomerated boards (Flores Yepes 2005). 203 samples and a Nei genetic diversity of 0.929) and Giant reed shoots have been consumed occa­ a weak diversity in North America, using 10 SSRs sionally, but they are bitter (Kunkel 1984; Rivera specifically developed from A. donax. The authors Núñez and Obón de Castro 1991). Rhizomes and surprisingly noted that sampling confusions with leaves have been consumed raw or cooked (Coyle Phragmites were possible, but they screened these and Roberts 1975) or dried and ground to make putative errors with control genotypes of Phragmites. bread (Chiej 1984). Giant reed stems and leaves In comparison to the results of other studies in the contain a wide range of harmful chemical sub­ Mediterranean, the results of the study calls for further stances, which probably serve as protection against uses of these specific SSRs in broader sampling in the insects and herbivores (Miles et al. 1993). The Mediterranean as well as for Asian populations using stems and leaves contain cardiac glycosides and newly collected fresh material. As a preliminary result, curare-mimetic indole alkaloids (Ghosal et al. Canavan et al. (2017) did not find genetic diversity in 1972), triterpenes and sterols (Chandhuri and South Africa using these 10 SSRs. To date, new gen­ Ghosal 1970), hydroxamic acid (Zuñiga et al. eration sequencing and large SNP datasets have not 1983), numerous other alkaloids and silica been used to estimate genetic diversity or resolve phy­ (Jackson and Núñez 1964). Recent studies have logenetic relationships within Arundo. shown that A. donax has great potential to be used in the development of new drugs for the treatment of human diseases (Al-Snafi 2015) 5. Impacts since it has antibacterial and antifungal properties (Shirkani et al. 2014). Due to its high fibre and 5.1. Uses and positive impacts low protein contents, leaves are not well digested; Arundo donax has been used for millennia for differ­ however, A. donax is used in a commercial diet ent purposes, such as for furnishings, wind instru­ supplied to cows to improve milk yield, which is ments, agriculture, construction, medicinal and attributed to the presence of elements reported as veterinary uses, food and energy. The aerial part of galactogogues (Behera et al. 2013). the giant reed has been used to make mats, lattices, More recently, several researchers have investigated and multiple household utensils, such as baskets and the phytoremediation potential of A. donax in heavy containers, based on the lightness and high stability of metal-contaminated soil. According to Cristaldi et al. these parts (Fernandes and Mendoça de Carvalho (2020), the plant showed good phytostabilization abil­ 2004; Martínez et al. 2014). Giant reed stems have ities and may also be suitable for phytoextraction with played an important role in Western culture through a longer exposure time. Another important current their influence on music development over the past use of the giant reed is biomass production for energy 5000 years ago. The reeds of woodwind instruments generation, either for the production of solid fuels for (clarinets, saxophones, Galician bagpipes, etc.) are thermal uses or for the production of second- 10 J. JIMÉNEZ-RUIZ ET AL. generation biofuels (Curt et al. 2012). Under optimal a diverse invertebrate community (Herrera and conditions, A. donax can grow 10 cm/day, which Dudley 2003). Another factor that influences the bio­ places it among the fastest growing plants. It can logical deficiencies of giant reed populations in com­ produce more than 20 tons of dry matter (DM) per parison to native plant populations is the decreased hectare (Perdue 1958; Bell 1997). In Italy, giant reeds availability of bare soil under A. donax for terrestrial can produce up to 60 tons DM/ha (Angelini et al. fauna and a greater possibility of desiccation 2005), and in California, this plant can produce up to (D’Antonio and Vitousek 1992). In addition, although 155 t DM/ha (Giessow et al. 2011). At present, numer­ the ranges of organic matter decomposition are simi­ ous studies are being carried out on the energy appli­ lar in A. donax and native plant communities, in areas cations of A. donax (Lemons e Silva et al. 2015). invaded by giant reeds, a double layer of litter is formed without interstitial spaces appropriate for the colonization of invertebrates (Bell 1997; Herrera and 5.2. Negative impacts Dudley 2003). In a recent study carried out by Arundo donax has become one of the most threatening Maceda-Veiga et al. (2016), the authors highlight an species in riparian habitats. The species can be con­ impoverishment of native flora and arthropod fauna sidered as a transformer sensu Richardson et al. in A. donax invaded habitats, suggesting that the pre­ (2000), due to its ability to deeply change the charac­ sence of giant reeds produce major changes in riparian ter, condition, form and nature of the invaded ecosys­ food webs displacing native riparian vegetation. tems at the landscape level. Richardson et al. (2000), in Altered or increased fire susceptibility of invaded their definitionof transformer species, cite A. donax as ecosystems an example in the category of excessive users of water The high biomass productivity of A. donax and and light resources. Changes in ecosystem functioning its low attractiveness to herbivores based on the can also be related to an increase in the regularity of harmful chemical substances it accumulates (Bell the fire regime induced by the high density of this 1997) lead to a large amount of fibrous leaves and species (Scott 1994; Brooks et al. 2003). stems that can reach 15.5 kg/m2 in some riparian Impacts on invaded biological communities communities in the USA (Giessow et al. 2011). In The dense root systems of giant reeds can inhibit comparison to native riparian vegetation, the giant the acquisition of water and nutrients by native spe­ reed has a lower moisture content and higher sur­ cies, while their aerial parts can form a dense cover face/volume ratio; thus, giant reed fields have that prevents the germination and growth of native a propensity to catch on fire, alter ecosystem pro­ species (D’Antonio and Vitousek 1992; Cabin et al. cesses and have adverse effects on native species, 1999). As a result, the uses of riparian ecosystems are both animals and plants (Frandsen and Jackson altered, producing negative effects on the biological 1994). Structurally, A. donax favours the transmis­ communities that the riparian environments host, i.e. sion of fire from the shrub layer to the tree layer a loss of habitats for animals, which entails a reduction due to its verticality. In addition, the rhizomes of in the intermediate trophic level and modification of giant reeds survive fires and regrow immediately the food chain. Specifically, birds find few opportu­ after a fire due to accumulated reserves, and they nities to shelter or nest in giant reed populations. The grow faster than native vegetation (Bell 1997). main stems of A. donax are vertical and lack Thus, fire contributes to the conversion of mixed a sufficiently robust horizontal structure to support riparian plant communities with native species to nests (Zembal 1998; U.S. Fish and Wildlife Service pure monocultures of A. donax, with a loss in 2002). Some studies in North America have shown biodiversity. that the cover of A. donax and the richness of birds An excessive user of water such as Vireo belli pusillus Coues and the threatened A. donax has the capacity to increase water loss in species Empidonax traillii extimus A.R. Philips in rivers due to its high water consumption (up to 2,000 l California (Bell 1997) are significantly and negatively of water per square metre) (Iverson 1994; Watts and related at all times of the year, and any increase in the Moore 2011). For example, in the Santa Margarita density of giant reed fields is accompanied by River Valley in California, it has been estimated that a decrease in the health and abundance of the avian the elimination of A. donax over an area of approxi­ community (Kissner 2004). Not surprisingly, inverte­ mately 405 hectares would save an amount of water brates, one of the main sources of food for birds, are equivalent to that consumed annually in an urban area 50% less abundant and diverse in giant reed fieldsthan of twenty thousand inhabitants (Bell 1997). According in native plant communities (Herrera and Dudley to Giessow et al. (2011), the leaf transpiration rate of 2003). The dense structure of giant reed populations A. donax, based on its water use value, is extremely limits the penetration of light and prevents the devel­ high (40 mm/day) compared to that of most other opment of a diverse shrub layer; thus, the habitat that plants in a field study carried out in southern is generated lacks sufficient heterogeneity to support California. In comparison with mixed riparian BOTANY LETTERS 11 vegetation, from 0.9 to 1.6 mm/day (Johns 1989), the management options, and the objectives and work water use of A. donax is much higher, which implies plan for their control need to be defined (Andreu a large potential water use reduction that could have and Vilà 2007). There are essentially three manage­ significant implications for both ecosystems and ment options for addressing invasive species: (a) pre­ humans. vent their entry (exclusion), both unintentional and Impacts on the nearby aquatic environmental intentional; (b) detect them rapidly and eradicate conditions them immediately upon entry (early detection and A. donax modifies riparian microclimates rapid response); and (c) minimize their impact with because it does not generate the structural cover containment and control strategies (Genovesi and necessary to provide sufficient shade to river-edge Shine 2004). These strategies are possible in the early habitats, so water is warmer, unlike the river-edge stages of an invasion, when populations are small or habitats in riparian forests of willow and poplar, localized. When invasive species occur at medium to which provide shade on riverbanks (Chadwick and large scales, the appropriate interventions to remove Associates 1992; Bell 1997; Dudley 2000). As them is to contain them and map them (Deltoro Torró a result, the riparian areas dominated by et al. 2012). On the other hand, Bradley (1997) pro­ A. donax tend to have much warmer water tem­ posed that control of invasive species should start in peratures, resulting in a decrease in dissolved oxy­ areas that are less invaded and progress gradually gen concentrations and lower abundance and towards the nucleus of the invasion, not before ecolo­ diversity of aquatic animals, including fishes gically restoring the former. (Dunne and Leopold 1978). In addition, this lack In the case of A. donax, that is already wide­ of plant coverage causes an increase in pH in the spread in southern Europe, one of the most impor­ shallow sections of rivers due to an increase in tant aspects to address for containing it, is to limit light and thus photosynthetic activity of algae. its spread downstream that occurs mainly during Finally, a high pH facilitates the conversion of flood events by the dispersal fragments of rhizomes ammonium (NH4) into ammonia (NH3) in and stems. Thus, management of A. donax is essen­ a cascade of harmful effects for aquatic species tially an intra-basin phenomenon, starting down­ and those that use this water (Chadwick and stream (Bell 1997). Furthermore, if this approach is Associates 1992; Bell 1993). combined with some control methods, the end An erosion promoter result is riparian areas devoid of vegetation and Arundo donax plants also negatively affect the vulnerable to erosion or reinvasion by other exotic hydrology and geomorphology of rivers, which species. Therefore, any elimination of A. donax also affects human activities (Quinn and Holt should be accompanied by restoration of the area, 2004). Giant reeds on riverbanks serve as walls, with the goal of recovering the characteristics of concentrating the energy of water flow in the the ecosystem (Moody and Mack 1988). Since the riverbed, which leads to the excavation of the control methods that are available differ in effec­ riverbed and collapse of riverbanks during floods tiveness, period of application, cost and environ­ (Else 1996; Dudley 2000). During these events, the mental impacts, planning is crucial to the success aerial parts and rhizomes of the monospecific and in each case. The duality of A. donax as an invasive very dense “forests” of A. donax can accumulate, species involved in the degradation of riverbanks forming dams, plugging bridges and preventing and, at the same time, as an energy crop must also the proper functioning of flood control structures, be considered when establishing control measures with potentially serious consequences. According to prevent its expansion into vulnerable areas. It is to Spencer et al. (2013), in comparison to rivers in recommended that A. donax should not be grown native forests, rivers with giant reeds along the near habitats vulnerable to its invasion and special river banks have a higher risk of river flooding measures should be taken during harvesting and (up to 19% more). Moreover, the masses of roots transport to avoid dispersal of stem fragments or (rhizomes) colonize riverbanks and fluvial ter­ rhizomes. A code of good practice could be races, altering the flow regime and modifying the adopted, similar to initiatives taken to limit the morphology of the riverbeds (Bell 1997). risk associated with non-native tree plantations (Brundu and Richardson 2016). Continuous sur­ veillance and monitoring, especially in vulnerable 6. Management areas, are essential for proper detection, for exam­ ple, using remote sensing techniques (Jiménez-Ruiz 6.1. Preventive strategies and considerations 2016) for the detection of species at low densities. Decisions regarding the population management of Dissemination of materials (guides, manuals, etc.) invasive species may be affected by various factors, to support the detection and control of the species such as the biology of the species and available would be beneficial. 12 J. JIMÉNEZ-RUIZ ET AL.

6.2. Manual removal be conducted at any time of the year, but it is less damaging to work in relatively dry conditions as Traditionally, A. donax is managed by manual the amount of substrate that adheres to the rhi­ removal (stripping) of the aerial parts of the zomes is reduced, minimizing soil loss. Rhizomes plants. However, this technique only serves as are generally found in the first 50 centimetres of a temporary control because over the mid-term substrate, although they can reach greater depths. (6 months later), new stems emerge from the Unfortunately, this methodology involves the rhizomes, and the species consolidates its domi­ extraction of a large amount of soil and substan­ nance over native riparian vegetation. Studies car­ tial alteration to the riparian environment, which ried out in several riparian areas of Europe must be restored to prevent erosion and recover indicate that because of sporadic stripping (not characteristic vegetation. Even under drought con­ continuous or repeated), there is actually an ditions with low moisture content, rhizomes increase of as much as 15% in the density of sprout after mechanical removal (Bell 1997). For reed stems with respect to the initial invasion this reason, it is important that periods between (Deltoro Torró et al. 2012). Other works describe clearings are short. If buds generated from rhi­ similar situations (USEPA 1997; Guthrie 2007). zomes are eliminated, then their reserves will be This method is labour intensive and can only be depleted quickly. With rhizome removal, it is pos­ applied over small areas; therefore, it is not gen­ sible to achieve almost complete eradication of erally or economically effective. A. donax, but it specifically requires that rhizomes and substrate are totally removed. Hence, reprofil­ ing and intensive recuperation efforts are neces­ 6.3. Mechanical control sary to counteract the negative effects involved. The mechanical control of A. donax consists of the complete removal of aboveground plant biomass with 6.4. Physical control heavy machinery. When this is carried out once a year, it is referred to as one-cut stumping (Quinn and Holt Physical control in invasive plant management 2008). This is not a very effective strategy, however, refers to the physical manipulation of plants or due to the tendency of the plant to re-sprout in their habitat (Enloe and Loewenstein 2015). This response to the loss of aboveground biomass. Field approach refers to a number of different techni­ study results outlined by Mota (2009) show that 5 ques, including controlling invasive plants by successive A. donax clearings every 20 days caused altering their environment, such as water level an 80% decrease in height of the re-sprouted stems manipulation, barriers with opaque textile cover­ and a reduction in number with respect to the initial ings, nutrient manipulation, and aeration. To con­ status. The results of Godé et al. (2008) also indicate trol A. donax, there are two main methodologies: that up to 9 successive clearings are necessary to elim­ textile coverings and flooding. These methods are inate one reed field. There is evidence that the elim­ very costly and are difficult to apply in many ination of re-sprouted stems additionally leads to settings; one could not use flooding in water- a decrease in belowground plant biomass (Sharma scarce regions, for example. et al. 1998). However, this species can grow in dark­ A textile covering is a completely opaque cover ness for 100 days (Decruyenaere and Holt 2005) or used on a cleared reed field (after cutting) to from rhizomes buried 1 m deep (Else 1996; Boose and deprive the plants of light. The rhizomes die due Holt 2002). It must also be taken into account that this to exhausting their reserves. Although San Martín species has a very high photosynthetic rate (Rossa et al. et al. (2019) found that one full calendar year was 1998), which causes the stems to become independent effective, other authors suggest that textile cover­ of the rhizome reserves once they emerge to the sur­ ings should be applied for two whole vegetative face. In fact, in terms of A. donax performance, seasons (Jiménez-Ruiz and Santín-Montanyá a positive correlation between biomass loss and several 2016). This method is suitable to control mono­ indirect negative effects (for example, reduced water specific A. donax plantations devoid of native efficiency) existed. This scenario could reduce the vegetation. competitive ability of the giant reed against native Flooding takes advantage of the intolerance of vegetation and lead to a reduction in its occupied A. donax rhizomes to anoxia. This procedure area (Jiménez-Ruiz and Santín-Montanyá 2016), requires first cutting the reed field and removing thereby facilitating more successful control of this aerial biomass. Then, a water cover of at least 20 species in Mediterranean (semi-arid) environments. centimetres must be established uninterrupted for The rhizome removal method consists of the at least 3 months. Flooding is a suitable method extraction of rhizomes from the soil with heavy for clumps close to a river and located at a level machinery after aerial biomass removal. This can slightly higher than the river. Studies from BOTANY LETTERS 13

Valencia (Spain) showed us that the ideal season assess the herbivory effecton giant reeds (Goolsby and to carry out flooding is in winter, during the Moran 2009, 2019; Moran and Goolsby 2009). Some vegetative dormancy of A. donax (Deltoro Torró potential herbivores that occur in Asia and the et al. 2012). Efficacy is high, up to 100% according Mediterranean area present high levels of herbivory to studies carried out in riparian areas of Spain effects; larvae of Cryptonevra sp. feed along the fibres (Mota 2009; Ollero 2010). of the leaves of new shoots, and adults of Tetramesa romana cause elongated galls around side shoots and induce internodal shortening (Kirk et al. 2003). In 6.5. Herbicide application Mediterranean Cortés et al. (2011a), Cortés et al. The management of Arundo donax with herbicides (2011b)) found that Rhizaspidiotus donacis Leonardi has mainly been carried out with broad-spectrum (Hemiptera: Diaspididae) has a significant impact on herbicides such as glyphosate (Spencer et al. 2009; A. donax growth since caterpillar feeding causes Puértolas et al. 2010). However, control with herbi­ a “witch’s broom” effect by reducing shoot growth, cides may be restricted in sensitive areas such as ripar­ reducing photosynthesis, and thinning of Arundo ian habitats. Therefore, managing invasive weed stands. In the USA, the biological control of species requires knowledge of both the invasive weed A. donax with herbivorous insects was also investi­ and the invaded ecosystem (Deltoro Torró et al. 2012). gated, and some arthropods were found to be asso­ More recently, specificglyphosate formulations and ciated with giant reeds but did not feed on the plants different active substances (asulam and trifloxysul­ (Herrera and Dudley 2003; Kirk et al. 2003). The furon) have been proposed to control this invasive Arundo wasp, Tetramesa romana Walker species (Odero and Gilbert 2012; San Martín et al. (Hymenoptera: Eurytomidae) and Arundo armoured 2019). Spencer et al. (2008) in California noted that scale Rhizaspidiotus donacis, native insects from the one foliar application of glyphosate solution at 3% or Mediterranean region, were released in North 5% was effective in controlling old populations of America with some success (Goolsby and Moran A. donax. In herbicide-sensitive habitats, such as in 2009; Goolsby et al. 2011). Ecophysiological responses riparian habitats, some studies show that glyphosate of different herbivorous insects on A. donax were injections into A. donax re-sprouts reduced the num­ assessed taking into account whether these species ber of live stems by 80% one year after application are capable of reducing the transpiration and growth (Spencer 2014). Bell (1997) reported that this species rates of giant reeds (Moore et al. 2010). The results was controlled with a 2 to 5% glyphosate solution on showed that in comparison to when groups of only the cut stems, and Jackson (1994) recommended Arundo wasp occur, when both herbivores, R. donacis a glyphosate solution of 1.5% for the control of adult and T. romana, occur in high densities at the same plants of A. donax as spot treatment with a foliar spray time, physiological processes of A. donax are reduced by ground equipment. Santín-Montanyá et al. (2013, (55% reduced biomass). T. romana directly affects the 2014) tested differentchemical treatments for the con­ carboxylation capacity of Rubisco, while R. donacis trol of A. donax in a field study carried out in the reduces the rate of electron transport (Moore et al. Harnina River Basin in Spain (Mediterranean cli­ 2010). However, a recent study conducted in Texas mate). Glyphosate (10 L per ha of formulated product) (USA) has shown that in natural habitats, freshly directly applied over-the-top of plants and glyphosate planted A. donax grows in dense clumps and prolifer­ applied on new sprouts were excellent means of con­ ates regardless of being infested by T. romana. The trolling the regrowth of A. donax. The combined tech­ authors concluded that T. romana under field condi­ nique of herbicide treatment and stem-cutting can be tions is a parasite that is well-adapted to A. donax and included in management programmes for does not kill the stems. Hence, according to Showler Mediterranean protected areas. However, studies and Osbrink (2018), exotic wasps cannot be consid­ available on the dosage and efficacy of glyphosate on ered effective biological control agents against A. donax are scarce in this kind of sensitive riparian A. donax in the USA. Among the prospects for areas (Lowrey and Watson 2004). The mid- and long- improving biological control, new species from the term effects of repeated applications of glyphosate on core native range of A. donax in Asia should be inves­ re-sprouting species, such as A. donax, are virtually tigated as source of biological control agents. It should unknown, and therefore, studies to assess the mid- be kept in mind that the implementation of this type of term prognosis for control are needed to test the control is a long process including rigorous risk ana­ usefulness and the sustainability of this technique. lysis to avoid non-target impacts (Paynter et al. 2020).

6.6. Biological control 6.7. Ecological control and restoration Concerning biological control, different studies have Native riparian species can help control A. donax as been carried out with the aim of releasing insects to they compete for resources effectively. Live branch 14 J. JIMÉNEZ-RUIZ ET AL. coverage is a new methodology that involves establish­ species (Spencer et al. 2008; Santín-Montanyá ing a dense vegetation cover of native riparian species et al. 2013, 2014; San Martín et al. 2019). that compete for resources and space. According to The control of Arundo donax should be encouraged Deltoro Torró et al. (2012), Salix species are the most through integrated management programmes that use suitable for this method, so they should be favoured biological control through natural enemies. For exam­ to optimize the results. These are abundant species in ple, Tetramesa romana Walker (Hymenoptera: most European fluvial courses, and willow is well Eurytomidae) and Rhizaspidiotus donacis, native adapted to floods and provides good protection for insects from the Mediterranean region, have been banks. These authors carried out one experiment in released in North America with some success Spain with Salix spp. (willow) that confirmedthat live (Moore et al. 2010; Goolsby and Moran 2019). grafted branches of willow should be planted in win­ Additionally, the combination of physical and ecolo­ ter months (during the dormancy period of giant gical control by native species can be employed on reed). Coffman (2007) confirmed that Salix species local populations with high ecological values where are capable of competing for space and resources other control options are not available. There are with A. donax, decreasing its productivity. On the some studies on Salix species competing for space other hand, plants such as Populus sp., Tamarix sp., and resources with giant reeds (Coffman 2007). Live Sambucus sp. and Cornus sp. can also be used but branch coverage with other plants, such as Populus sp., with less success (Deltoro Torró et al. 2012). Tamarix sp., Sambucus sp. and Cornus sp., have also Coverage with live branches is very effective, but been used with less success (Deltoro Torró et al. 2012). there are clear conditions that make it successful: A multidisciplinary approach is necessary to first, stem cutting must be carried out, and second, address the damage posed by this invasive species. the riverbanks need to have a shallow gradient to Greenhouse and field experiments are important to maintain some level of flooding (which A. donax determining the control options for A. donax at early does not tolerate). These results highlight the impor­ stages of invasion and to measure the combination of tance of restoration with native species after the multiple techniques in short-term and long-term stu­ removal of A. donax, especially in nutrient-rich dies. New studies to assess the utility of measures in environments. combination with other methodologies are needed. In addition, cost-effectiveness should receive more con­ sideration by researchers and administrations that 6.8. Integrated management manage nature conservation. Integrated weed management can offer a solution to control or at least contain this species by limit­ 7. Cost analysis of management ing its spread. At present, giant reeds can be con­ The costs and possible impacts on the environment trolled by mechanical treatments such as stem differ between different control methods in cutting and removal by digging, although these a significant way (Table 4). The control of giant measures may be ineffective and/or insufficient reeds is possible with traditional methods, such as due to the high reproduction rate of this plant. the use of herbicides or the mechanical extraction of Herbicides, which are widely used in agriculture, rhizomes. Nevertheless, it is also possible to control have certain disadvantages when used in the nat­ A. donax with other methods less frequently used, ural environment, mainly due to their low speci­ such as opaque tarps, prolonged floodingor ecological ficity and the possibility of their accumulation in restoration with native riparian species. Given that the soil and organisms. The selection of herbicides in different methods differ in their unintended effects on an integrated programme is fundamental to ensur­ the environment and in their application costs, the ing effective control. Herbicides with short half- choice of the most suitable method will depend on lives or herbicides at low doses are commonly multiple variables from regulatory aspects to the types used so that the environment can easily recover of interventions, including the characteristics of the after treatment. Chemical treatment is cheaper but giant reed population, the location of the action and not always effective in controlling this species and the potential to apply additional treatments in succes­ may not be the best option in herbicide-sensitive sive years. The most economical method is spraying habitats such as riparian areas. Mechanical treat­ glyphosate on sprouts post-cutting and is approxi­ ments are often effective although more expensive mately 1.28 € per m2 (including three stem-cuttings). than chemical treatments. Recent research in tem­ According to Deltoro Torró et al. (2012), mechanical perate environments has shown that in compari­ treatment is very expensive at 21.97€ per m2 (rhizome son to other methods, the joint application of extraction with heavy machinery). With integrated mechanical and chemical (herbicide) treatments management, depending on the treatment, re-cutting is cheaper and more effective at eradicating this can increase the effectiveness of the initial treatment BOTANY LETTERS 15

Table 4. Recommendations for the method selected. Mediterranean riparian habitats. Optimal manage­ Control Time of ment and control measures must be applied to Methods Use application Benefits mitigate the negative impacts of this species in Cutting In small areas, Any time. The substrate when it is The best and close freshwater ecosystems. Currently, there is a need necessary to results at the vegetation to increase the efficiency of current control tech­ intervene end of are not quickly or it is summer, modified. niques, and this requires a better understand of not possible to when No use of the invasive potential of this species and its use other rhizomes are chemical methods. actives. products. responses to different control methods. In fact, Low cost. the difficulty in controlling this species lies in its Rhizome In adults In summer, with No use of morphology, modes of growth and propagation extraction populations dry chemical with the conditions to products. (vegetative growth), physiology and tolerance to rhizomes on avoid the soil Close a wide variety of ecological conditions. Most of surface loss. vegetation not modified. the actions that have been carried out to control Good control. this species have not been successful since they Herbicide In small and During the Low soil sprayed homogeneous vegetative alterations. have been based on temporarily eliminating it. populations period. Good control. Control measures against A. donax involve herbi­ far-off water Low cost. courses. cidal control, biomass cutting and removal, biolo­ Cutting + In extended and Cutting in spring Low soil gical control and ecological methods. Based on Herbicide homogeneous and Herbicide alterations. recent results, biological control should be encour­ sprayed on populations on sprout in Good control. sprout summer. Less aged by competent authorities in Europe for weed unintended management as a useful integrated management effects. Cutting + All types of During the Low soil tool (Shaw 2007). At present, integrated manage­ Herbicide populations vegetative alterations. ment programmes, in addition to continuous tech­ brushed period. Good control. onto sprout No derived nological change, natural area manager effects. participation, technology transfer, and the policy Less herbicide environment, are key components for achieving consumption. control of this species. Specific programmes Textile In small and Any time Not use of should be developed to increase knowledge of covering homogeneous chemical populations products. A. donax biology and the efficiency of control Good control. methods. High cost. Covering of In populations End of summer Restorations live close to river with native branches species. (ecological Good control. Acknowledgments control and Medium soil restoration) alterations. The authors wish to thank anonymous reviewers and to High cost. Régine Verlaque for SEM figures.

Disclosure statement 10-fold but represents an additional cost that ranges between 10 and 40%. No potential conflictof interest was reported by the authors.

8. Conclusion Notes on contributors Arundo donax is an introduced, well-established inva­ Jesús Jiménez-Ruiz is a plant ecologist with interests in sive species in southern Europe. In general, the genus ecology and management of biological invasions, who is Arundo shows low genetic diversity in its invaded currently working in his PhD thesis about the biology and management of A. donax at the Polytechnic University of range, and some aspects of the giant reed, such as its Madrid. He is also a researcher at the National Institute for phylogenetic relationships within Arundo, are still Agricultural and Food Research (INIA). He contributed to unclear. It propagates via rhizome elongation and the sections of ecology and biology (phenology and physiol­ fragmentation, while the flowers of the large inflores­ ogy). He also coordinated the team during writing the cence are sterile in the invaded range. In addition, manuscript and reviewed the final draft. giant reeds have been used in Mediterranean areas to Laurent Hardion is an ecologist working in plant systema­ address the needs of local people, and currently, they tics, evolution, and biological conservation. He led his PhD can be cultivated as bioenergy crops. thesis on the systematics of the genus Arundo at Aix- Marseille University, CNRS. He is currently lecturer at The giant reed is invasive in riparian areas and University of Strasbourg, CNRS. He contributed to the sec­ its uncontrolled presence can reduce native plant tions taxonomy, distribution and status, reproductive biol­ species richness, which is damaging for ogy and genetic diversity. 16 J. JIMÉNEZ-RUIZ ET AL.

Juan Pablo Del Monte is lecturer at the Polytechnic Bell, GP. 1997. Ecology and management of Arundo donax, University of Madrid (UPM). He is a botanist agronomist and approaches to riparian habitat restoration in working in biology and ecology of weed population Southern California. In J H Brock, M Wade, P Pysek, dynamics. He has also experience in agronomy and crop D Green, editors. Plant invasions: studies from North production. He contributed to the sections impacts and America and Europe. Netherlands: Backhuys Publishers; uses. p. 103–113. Boland, JM. 2006. The importance of layering in the rapid Bruno Vila is lecturer at the University of Aix-Marseille and spread of Arundo donax (giant reed). Madroño. 53 the curator of MARS herbarium. He is working in plant (4):303–312. doi:10.3120/0024-9637(2006)53[303: systematic and in plant conservation. He is also working in TIOLIT]2.0.CO;2. urban ecology where he is studying biodiversity organiza­ Boland, JM. 2008. The roles of floods and bulldozers in the tion according to urbanization. He contributed to the sec­ break-up and dispersal of Arundo donax (giant reed). tions taxonomy, distribution and status, reproductive Madroño. 55(3):216–222. doi:10.3120/0024-9637- biology and genetic diversity. 55.3.216. Mª Inés Santín-Montanyá is a researcher biologist at the Bolòs, OD, J Vigo. 2001. Flora dels Països Catalans. Vol. I National Institute for Agricultural and Food Research and (Monocotiledònies). Barcelona: Editorial Barcino. Technology (INIA). She is working in weed-crop competi­ Boose, AB, JS Holt. 2002. Environmental effects on asexual tion, studying the ecology of weed population dynamics, the reproduction in Arundo donax. Weed Res. 39 control of emergent weed species and sustainable agricul­ (2):117–127. doi:10.1046/j.1365-3180.1999.00129.x. ture. She contributed to the sections of management and Bradley, J. 1997. 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